Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
???displayArticle.abstract???
While we understand how stimuli evoke sudden, ballistic escape responses, like fish fast-starts, a precise pathway from sensory stimulation to the initiation of rhythmic locomotion has not been defined for any vertebrate. We have now asked how headskin stimuli evoke swimming in hatchling frog tadpoles. Whole-cell recordings and dye filling revealed a nucleus of ∼20 trigeminal interneurons (tINs) in the hindbrain, at the level of the auditory nerve, with long, ipsilateral, descending axons. Stimulation of touch-sensitive trigeminal afferents with receptive fields anywhere on the head evoked large, monosynaptic EPSPs (∼5-20 mV) in tINs, at mixed AMPAR/NMDAR synapses. Following stimuli sufficient to elicit swimming, tINs fired up to six spikes, starting 4-8 ms after the stimulus. Paired whole-cell recordings showed that tINs produce small (∼2-6 mV), monosynaptic, glutamatergic EPSPs in the hindbrain reticulospinal neurons (descending interneurons, dINs) that drive swimming. Modelling suggested that summation of EPSPs from 18-24 tINs can make 20-50% of dINs fire. We conclude that: brief activity in a few sensory afferents is amplified by recruitment of many tINs; these relay summating excitation to hindbrain reticulospinal dINs; dIN firing then initiates activity for swimming on the stimulated side. During fictive swimming, tINs are depolarised and receive rhythmic inhibition but do not fire. Our recordings demonstrate a neuron-by-neuron pathway from headskin afferents to the reticulospinal neurons and motoneurons that drive locomotion in a vertebrate. This direct pathway, which has an important amplifier function, implies a simple origin for the complex routes to initiate locomotion in higher vertebrates.
Aoki,
Locomotion elicited by pinna stimulation in the acute precollicular-postmammillary decerebrate cat.
1981, Pubmed
Aoki,
Locomotion elicited by pinna stimulation in the acute precollicular-postmammillary decerebrate cat.
1981,
Pubmed
Brodfuehrer,
From stimulation to undulation: a neuronal pathway for the control of swimming in the leech.
1986,
Pubmed
Cangiano,
Fast and slow locomotor burst generation in the hemispinal cord of the lamprey.
2003,
Pubmed
Clarke,
Interneurones in the Xenopus embryo spinal cord: sensory excitation and activity during swimming.
1984,
Pubmed
,
Xenbase
Crapse,
Corollary discharge across the animal kingdom.
2008,
Pubmed
Dubuc,
Initiation of locomotion in lampreys.
2008,
Pubmed
Edwards,
Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish.
1999,
Pubmed
Goulding,
Circuits controlling vertebrate locomotion: moving in a new direction.
2009,
Pubmed
Grillner,
Neural bases of goal-directed locomotion in vertebrates--an overview.
2008,
Pubmed
Hayes,
The anatomy of two functional types of mechanoreceptive 'free' nerve-ending in the head skin of Xenopus embryos.
1983,
Pubmed
,
Xenbase
Jordan,
Descending command systems for the initiation of locomotion in mammals.
2008,
Pubmed
Kahn,
The central nervous origin of the swimming motor pattern in embryos of Xenopus laevis.
1982,
Pubmed
,
Xenbase
Korn,
The Mauthner cell half a century later: a neurobiological model for decision-making?
2005,
Pubmed
Kyriakatos,
Initiation of locomotion in adult zebrafish.
2011,
Pubmed
Li,
Dorsal spinal interneurons forming a primitive, cutaneous sensory pathway.
2004,
Pubmed
,
Xenbase
Li,
Specific brainstem neurons switch each other into pacemaker mode to drive movement by activating NMDA receptors.
2010,
Pubmed
,
Xenbase
Li,
Spinal inhibitory neurons that modulate cutaneous sensory pathways during locomotion in a simple vertebrate.
2002,
Pubmed
,
Xenbase
Li,
Defining classes of spinal interneuron and their axonal projections in hatchling Xenopus laevis tadpoles.
2001,
Pubmed
,
Xenbase
Li,
Persistent responses to brief stimuli: feedback excitation among brainstem neurons.
2006,
Pubmed
,
Xenbase
Li,
The spinal interneurons and properties of glutamatergic synapses in a primitive vertebrate cutaneous flexion reflex.
2003,
Pubmed
,
Xenbase
Li,
Locomotor rhythm maintenance: electrical coupling among premotor excitatory interneurons in the brainstem and spinal cord of young Xenopus tadpoles.
2009,
Pubmed
,
Xenbase
Matesz,
The motor column and sensory projections of the branchial cranial nerves in the frog.
1978,
Pubmed
Noga,
The effect of selective brainstem or spinal cord lesions on treadmill locomotion evoked by stimulation of the mesencephalic or pontomedullary locomotor regions.
1991,
Pubmed
Noga,
Locomotion produced in mesencephalic cats by injections of putative transmitter substances and antagonists into the medial reticular formation and the pontomedullary locomotor strip.
1988,
Pubmed
Poulet,
New insights into corollary discharges mediated by identified neural pathways.
2007,
Pubmed
Roberts,
Pineal eye and behaviour in Xenopus tadpoles.
1978,
Pubmed
,
Xenbase
Roberts,
How does a nervous system produce behaviour? A case study in neurobiology.
1990,
Pubmed
,
Xenbase
Roberts,
Conducted impulses in the skin of young tadpoles.
1969,
Pubmed
Safronov,
High-resolution single-cell imaging for functional studies in the whole brain and spinal cord and thick tissue blocks using light-emitting diode illumination.
2007,
Pubmed
Soffe,
Defining the excitatory neurons that drive the locomotor rhythm in a simple vertebrate: insights into the origin of reticulospinal control.
2009,
Pubmed
,
Xenbase
Soffe,
Roles of Glycinergic Inhibition and N-Methyl-D-Aspartate Receptor Mediated Excitation in the Locomotor Rhythmicity of One Half of the Xenopus Embryo Central Nervous System.
1989,
Pubmed
,
Xenbase
Stein,
Motor systems, with specific reference to the control of locomotion.
1978,
Pubmed
Stephenson-Jones,
Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection.
2011,
Pubmed
ten Donkelaar,
Cells of origin of descending pathways to the spinal cord in the clawed toad (Xenopus laevis).
1981,
Pubmed
,
Xenbase
Viana Di Prisco,
The trigeminal sensory relay to reticulospinal neurones in lampreys.
2005,
Pubmed
Vinay,
Evidence for the existence of a functional polysynaptic pathway from trigeminal afferents to lumbar motoneurons in the neonatal rat.
1995,
Pubmed
